Analysis of 90 Mb of the potato genome reveals conservation of gene structures and order with tomato but divergence in repetitive sequence composition
- Wei Zhu†1, 4,
- Shu Ouyang†1,
- Marina Iovene2,
- Kimberly O'Brien1, 5,
- Hue Vuong1,
- Jiming Jiang2 and
- C Robin Buell3Email author
© Zhu et al; licensee BioMed Central Ltd. 2008
Received: 14 January 2008
Accepted: 13 June 2008
Published: 13 June 2008
The Solanaceae family contains a number of important crop species including potato (Solanum tuberosum) which is grown for its underground storage organ known as a tuber. Albeit the 4th most important food crop in the world, other than a collection of ~220,000 Expressed Sequence Tags, limited genomic sequence information is currently available for potato and advances in potato yield and nutrition content would be greatly assisted through access to a complete genome sequence. While morphologically diverse, Solanaceae species such as potato, tomato, pepper, and eggplant share not only genes but also gene order thereby permitting highly informative comparative genomic analyses.
In this study, we report on analysis 89.9 Mb of potato genomic sequence representing 10.2% of the genome generated through end sequencing of a potato bacterial artificial chromosome (BAC) clone library (87 Mb) and sequencing of 22 potato BAC clones (2.9 Mb). The GC content of potato is very similar to Solanum lycopersicon (tomato) and other dicotyledonous species yet distinct from the monocotyledonous grass species, Oryza sativa. Parallel analyses of repetitive sequences in potato and tomato revealed substantial differences in their abundance, 34.2% in potato versus 46.3% in tomato, which is consistent with the increased genome size per haploid genome of these two Solanum species. Specific classes and types of repetitive sequences were also differentially represented between these two species including a telomeric-related repetitive sequence, ribosomal DNA, and a number of unclassified repetitive sequences. Comparative analyses between tomato and potato at the gene level revealed a high level of conservation of gene content, genic feature, and gene order although discordances in synteny were observed.
Genomic level analyses of potato and tomato confirm that gene sequence and gene order are conserved between these solanaceous species and that this conservation can be leveraged in genomic applications including cross-species annotation and genome sequencing initiatives. While tomato and potato share genic features, they differ in their repetitive sequence content and composition suggesting that repetitive sequences may have a more significant role in shaping speciation than previously reported.
The potato (Solanum tuberosum) tuber is a specialized underground storage organ that develops from modified stems termed stolons. Although the tuber is primarily composed of starch, it also contains high levels of proteins and due to its importance as a food source, a prime focus in potato research has been tuber quality [1–6]. Another key focus in potato research is disease resistance as potato is susceptible to several pathogens including Phytophthora infestans, the causal agent of late blight of potato. Molecular and genomic approaches, coupled with initial genetic mapping data, have identified resistance genes in potato against this pathogen [7–11] including a potentially viable commercial form of resistance to late blight conferred by the RB gene identified in the wild potato species, Solanum bulbocastanum, which can confer resistance to a wide range of P. infestans isolates.
Genomic resources for potato have been developed including Expressed Sequence Tag (ESTs; [12–14]), bacterial artificial chromosome (BAC) clone libraries [15, 16], microarray platforms [2, 17], and a dense genetic map . These resources have been utilized in studies on potato physiology, development, responses to abiotic and biotic stress, polyploidy, comparative genomics as well as enhancement of genetic maps [2, 17, 19–26]. The potato genome is reported to be 798–931 Mb  and with the availability of improved sequencing technologies, coupled with decreased fiscal constraints on genome sequencing, an international consortium to sequence the potato genome has been established . The Potato Genome Sequencing Consortium (PGSC) is focused on generating an initial draft sequence of the potato genome using a BAC-by-BAC approach followed by a finishing phase. The PGSC is enabled by the availability of two resources, a dense genetic map for potato  and an anchored Amplified Fragment Length Polymorphism-fingerprinted BAC library .
Collectively, the Solanaceae family is one of the world's most important vegetable families as species are grown for their tubers (potato), fruits (tomato, pepper, eggplant), leaves (tobacco), and ornamental features (petunia, Nicotiana species). In 2006 in the U.S., potato production was valued at $3.2 billion with tomato, tobacco, and pepper production valued at $1.6 billion, $1.2 billion, and $686 million, respectively . While the cultivated species have been bred for these diverse agronomic traits, genome sequence analysis has indicated that these species share to a large extent not only genes  but also gene order (synteny) between their genomes [31–35]. While major classes of repetitive sequences are conserved among some Solanaceae species [36, 37], lineage-specific repetitive sequences have been reported, suggesting divergence of this fraction of the genome has occurred through evolution [36–42]. With the availability of large genomic datasets for two Solanaceae species, tomato and potato, the extent of sequence conservation as well as synteny can be addressed in a more robust manner. In this study, we report on the generation of the first large set of genomic sequences from the potato genome along with characterization of these sequences with respect not only to the potato genome landscape but also in a comparative manner with genome sequences from tomato. We further compared our potato genome sequences with sequences from the collective Solanaceae transcriptome to determine the extent to which available solanaceous sequences can be used to cross-annotate the potato genome.
Results and Discussion
Characteristics of the potato genome
Statistics of BAC end sequence data in comparison to that of complete plant genomes.
Average Length (nucleotides)
Two sets of potato BACs were targeted for sequencing, BACs anchored on chromosome 6 and BACs putatively syntenic with tomato (Additional Data Files 1 and 2). A total of 22 potato BACs were sequenced in this study and we were able to generate 13 potato BACs in phase 2 and 3 which have ordered, oriented contigs allowing for gene annotation. Additionally, five complete (phase 3) potato BACs available in Genbank from other S. tuberosum BAC libraries were included in this study.
Features of potato and tomato BAC sequences.
Potato Syntenic BACs
Tomato Syntenic BACs
Random Potato BACs
Exons per gene
Exon GC content
Intron GC content
Gene GC content
CDS/ORF GC content
First position GC
Second position GC
Third position GC
Sequence level conservation within the Solanaceae and its use in annotation of the potato genome
Extent of transcript support for annotated potato genes among the Solanaceae transcriptome dataset.
Including Potato TAb
Excluding Potato TAc
Synteny between potato and tomato
Previous studies with the Solanaceae [31, 33, 34, 50, 51] identified synteny between a number of Solanaceae species including potato and tomato. These studies utilized genetic markers and showed, albeit at a low resolution, conservation of gene order between potato and tomato. With the pending availability of the tomato genome sequence, we were interested in determining the extent of synteny between tomato and potato to assess whether tomato genome sequences can be used 1) to identify syntenic potato BACs for the potato genome sequencing initiative, 2) to provide contig order and orientation information for potato BACs sequenced to draft level, and 3) to provide as a "reference genome" for structural annotation of the potato genome.
Statistics on syteny between potato and tomato.
Match Length (bp)
Synteny Length (bp)
Synteny Length Difference (bp)
No. Gene Pairs
Repetitive content of the potato genome
Classification of repetitive sequences in the potato and tomato genome.
Ribosomal RNA genes
A significant amount of rDNA sequences (3.99%) were detected in the tomato BES dataset while rDNA sequences found in potato BAC ends (0.50%) were minimal in comparison. The tomato BES were derived from three libraries constructed with Eco RI, Hin dIII and Mbo I restriction enzymes while the potato BES were derived from two libraries constructed with Eco RI and Hin dIII. Multiple Eco RI and Mbo I restriction sites are present in both the tomato and potato rDNA sequence (data not shown) and for the potato BES dataset, the ratio between Eco RI BES and Hin dIII BES is 0.70 (57,778/82,481). Therefore, there should be ample detection of rDNA sequences in the potato BES datasets suggesting that there may be a bias in overall rDNA content between potato and tomato. Analysis of individual libraries for potato and tomato confirmed this finding (Additional Data File 4). The rDNA sequences in potato are reported to be on chromosomes 1 (5S; ) and 2 (45S; nucleolar organizing region, [54, 55]). It has been reported that rDNA content differs between potato and tomato with tomato having more rDNA than potato [36, 56]. Thus, it is likely that the sampling of rDNA sequences, as reflected by BES survey sequencing, is reflective of a true rDNA content difference in the nuclear genomes of tomato and potato.
To contrast with the short BES-derived genome sequence, a total of 18 phase 2 and 3 potato BACs (2.20 Mb) and 16 tomato BACs (1.69 Mb, in 8 contigs/BACs) were analyzed for repetitive sequence content. Overall, the repetitive sequence fractions identified were comparable between potato and tomato BACs (25.90% vs. 22.30%). Similar to that observed with the BES datasets, more than half of the repeats identified in both the potato and tomato BAC sequences were unclassified (13.51% vs. 11.61%, respectively) while retrotransposon sequences were the most abundant characterized repetitive element in both potato and tomato BACs (9.58% vs. 8.32%, respectively). As observed with the potato BES dataset, there were more Ty3-gypsy type retrotransposons than Ty1-copia retrotransposons (3.34% vs. 1.92%) in the potato BACs. However, in contrast to that observed in the tomato BES dataset, more Ty1-copia than Ty3-gypsy type retrotransposons were present in tomato BAC sequences (0.99% Ty3-gypsy vs. 3.48% Ty1-copia). Interestingly, more transposon sequences were found in potato and tomato BAC sequences (2.69% vs 2.35%, respectively) than in the BES datasets (1.32% potato vs 1.39% tomato BES). Not surprisingly, there were almost no telomeric-related repetitive sequences or rDNA sequences identified in either potato or tomato BAC sequences. The lack of these sequences in the limited BACs examined is reflective of the euchromatic nature of the tomato BACs and their syntenic potato counterparts.
For potato, the overall percentages of repetitive sequences identified in the BAC and BES datasets were relatively comparable (total repeats: BES 34.18% vs. BAC 25.90%) and is consistent with the fact that nearly half of the potato BACs sequenced in this study (7/19 BACs) were randomly selected and reflect characteristics of the entire potato BAC library and genome. However, for tomato, the overall composition of repetitive sequences in the BES and BAC datasets differed significantly (total repeats: BES 46.29% vs. BAC 22.30%). This is attributable to the fact that the BACs sequenced by the Tomato Genome Initiative  are preferentially selected from the euchromatic regions which contain less repetitive sequences than the heterochromatin regions of the genome .
Certainly, identification of differences in relative composition of repetitive sequences between potato and tomato is not novel, however, the large difference in total repetitive sequence content between tomato and potato is surprising considering that these two Solanum species diverged less than 12 Million Years Ago . The haploid genome size of tomato and potato differ with tomato reported to be 950 Mb while that of potato is 865 Mb (range 798–931 Mb; ). Thus, with 34.2% and 46.3% repetitive sequences in potato and tomato, respectively, the total repetitive sequence space within the whole genome would be 296 Mb (potato) and 440 Mb (tomato) leaving a comparable non-repetitive fraction of their genomes of 569 Mb in potato and 510 Mb in tomato. This higher level of repetitive sequence is consistent with our finding of a higher frequency of matches within the potato BES to a Solanaceae EST compared to the tomato BES (5.5% vs 3.8%, respectively). Thus, the repetitive sequences within their respective genomes not only diverged in terms of classes of sequences but also in number leading to a biased amplification of repetitive sequences in tomato compared to potato.
We report on a large set of genomic sequences representing 10.2% of the potato genome. Using comparative analyses with solanaceous species we were able to demonstrate the utility and power of comparative genomics to not only annotate potato genomic sequences but also to assist in genome sequencing efforts among the Solanaceae. While we were able to confirm synteny on a genome scale with segments of the tomato and potato genome > 100 kb, we have also demonstrated that synteny is not absolute and that insertions/deletions as well as micro-inversions have occurred since the divergence of potato and tomato. More strikingly, the repetitive sequence content and composition of potato and tomato have diverged with impacts seen on genome architecture at both the macro- and the micro-level as evidenced through differences in telomeric-repetitive sequences and rDNA content and in interruption of synteny through transposition of retrotransposons. Our data are consistent with previous reports on repetitive sequences [36–42] which show divergence of this fraction of the genome within the Solanaceae. These data clearly suggest that while these two solanaceous genomes can be cross-leveraged for analysis of gene content and order, they are not interchangeable with respect to all genomic features.
Sequences used in this study
Potato genome sequences (BES and BAC sequences) generated in this study are described below. Tomato BAC end sequences (305,429 sequences, 273.99 Mb total) were downloaded from the GSS division of Genbank on Nov. 12, 2007. EST collections for the solanaceous species were obtained from the TIGR Plant Transcript Assemblies project ([49, 58]; dated on 11/20/2007). The release versions used in this study are shown in Additional Data File 3. The tomato BAC sequences were downloaded from Genbank and SGN  on Oct. 29, 2007, and were merged into a set of 518 unique tomato BACs.
The RHPOTKEY BAC library was constructed from RH parent Solanum tuberosum var. RH89-039-16 using Hin dIII and Eco RI restriction enzymes (C. Bachem, Pers. Comm., ). Templates were prepared using a high throughput alkaline lysis method, sequenced on ABI 3730 × l sequencers using TF and TR primers using standard high throughput sequencing methods, and processed with Paracel Trace Tuner . All sequences were trimmed to remove vector, low-quality, and E. coli sequences using Lucy  and iterative runs of the TIGR Seqclean Tool . All potato BAC end sequences have been submitted to the GSS division of Genbank with accession numbers EI367122-EI91525, EI812397-EI846477, and ER788642-ER870415.
Potato BAC DNA was isolated using the Sigma Phase Prep BAC DNA kit (Sigma, St Louis, MO) according to manufacturer's protocol. Approximately 7.5 ug was used for library construction. Samples were treated overnight with 100 U of Plasmid-Safe ATP-Dependent Dnase (Epicenter, Madison, WI) to remove contaminating bacterial chromosomal DNA and nebulized. Sheared DNA was precipitated and polished using the DNATerminator End Repair Kit following the manufacturer's protocol (Lucigen, Middleton, WI). Samples were electrophoresed on a 1.0% low melting point agarose and fragments in the range of 3–6 kb were selected for ligation into the pSMART-HCKan vector (Lucigen, Middleton, WI). Templates from the shotgun libraries were sequenced using TX and TY primers as described by Lucigen using standard high throughput sequencing methods on ABI 3730 × l sequencers. Sequences were trimmed as described above for the BAC end sequences and assembled with Celera Assembler . Potato BAC sequences have been deposited in the HTG division of Genbank under accession numbers AC204499, AC204500, AC206931-AC206936, AC209514-AC209520, AC212037, AC212316, AC212552, and AC212966.
Fluorescent in situ hybridization
Potato variety Katahdin (2n = 48) and a haploid clone USW1 (2n = 24) derived from Katahdin were used in FISH analysis. The FISH procedure followed published protocols . Briefly, BAC DNA was isolated and labeled with Biotin-UTP. Hybridization signals were detected FITC-conjugated avidin. Chromosomes were counterstained by 4', 6-diamidino-2phenylindole (DAPI) and were pseudocolored in red. Images were captured digitally using a SenSys CCD (charge coupled device) camera attached to an Olympus BX60 epifluorescence microscope. The CCD camera was controlled using IPLab Spectrum v3.1 software (Signal Analytics, Vienna, VA) on a Macintosh computer.
The potato BACs and the syntenic tomato contigs were annotated in parallel. First, the potato and tomato BACs were masked for repetitive sequences using RepeatMasker with a modified TIGR Solanum Repeat Database v3.3 in which miniature inverted repeat transposable elements (MITEs) and non-transposable element-related repeats were excluded. Second, gene models were predicted using the ab initio gene finder FGENESH (dicot matrix; ) and were updated using transcript evidence (ESTs, cDNAs) with the Program to Assemble Spliced Alignments . Moreover, the gene structures were manually inspected and some aberrant models, e.g., overlapping/nested or short (< 50 amino acids) genes, were removed. Third, gene function was assigned based on sequence identity to proteins within an in-house non-redundant protein database and/or the presence of Pfam domain(s), in a similar manner as reported previously for annotation of the rice genome . Gene functions were classified into three categories: "known/putative", "expressed" or "hypothetical". Genes in which functional assignments could be assigned based on sequence similarity to a known protein or the presence of a Pfam domain above the trusted cutoff score (unique for each Pfam domain) were annotated as encoding either a known or putative protein; the remaining gene models for which no sequence similarity or Pfam domain evidence was available were annotated as encoding an "expressed protein" if cognate transcript support was available or "hypothetical protein" if cognate transcript support was absent.
The solanaceous transcript assemblies (downloaded from ) were searched against the potato BACs using the program GAP2 . High quality alignments were defined as having sequence identity ≥ 80% and coverage ≥ 70% of the length of the Transcript Assembly. Only alignments meeting these cutoff criteria were used in downstream analyses and a solanaceous transcript was considered to support the ab initio-based annotation if the spliced alignment of the transcript overlapped a minimum of 100 bp with the gene model.
Identification of candidate syntenic tomato sequences
We utilized two methods to identify potential syntenic tomato-potato sequences. For Set I, tomato BACs were downloaded either from Genbank or SGN  and 14 overlapping tomato BACs were merged into 6 contigs to facilitate alignment and mapping to the potato BES. The potato BES were repeat masked and mapped to the tomato contigs using the program BLASTN with an E value cutoff of ≤ 1e-5. Paired potato BES were selected if they mapped to the same tomato contig in the correct orientation and within an expected intervening distance (50~200 kb). In total, 52 potato BACs were identified as candidate syntenic clones; eight potato BAC clones were sequenced. It is possible that BACs either from chromosome 6 or other chromosomes in the potato genome are syntenic with tomato BACs available in the public domain. To address this issue, we utilized the ab initio gene finder, FGENESH  to predict genes in the 18 phase 2 and 3 potato BACs and the 518 tomato BACs and searched these gene models against each other using BLASTP. The DAGchainer program  was employed to identify syntenic gene blocks between the potato and tomato contigs; putative syntenic potato-tomato BACs identified with this approach were termed Set II.
Synteny between tomato and potato was examined at the nucleotide and the protein level. Genomic comparisons at the nucleotide level utilized the NUCMER program . Syntenic gene blocks between potato and tomato contigs were generated by the BLASTP/DAGchainer  pipeline using the predicted protein sequences from the semi-automated annotation pipeline with improved gene structures/models rather than the ab initio FGENESH predictions.
Repeat database construction
Publicly available sequences were searched to expand our existing TIGR Solanum Repeat Database [69, 70]. New Solanaceae repetitive sequences were first collected from Genbank and used to update the TIGR Solanaceae Repeat Database. The TIGR Solanaceae Repeat Database was then searched against Solanum BAC sequences (41 non-tomato Solanum BACs and 301 tomato BACs, 40.05 Mb total sequence) from GenBank and the SGN  using RepeatMasker ( with a cut-off score of 225 which should not yield false positives). Sequences within the BACs that matched a repetitive sequence in the TIGR Solanaceae Repeat Database with ≥ 75% identity and ≥ 95% overall length were excised, coded , and combined with other Solanum repetitive sequences in the TIGR Solanaceae Repeat Database. Lastly, the same set of Solanum BAC sequences was searched with the de novo repetitive sequence finding algorithm, RepeatScout . Low-complexity sequences in the RepeatScout-generated fasta-formated sequence output were filtered out. To prevent inclusion of paralogous protein coding genes, all RepeatScout-generated sequences with similarity to known proteins or Pfam domains were identified and removed. All remaining repetitive sequences were coded based on the similarity with known repetitive sequences and added to the Solanum repetitive sequences to create the TIGR Solanum Repeat Database v3.3.
Repetitive sequence identification
Potato and tomato BAC end sequences (BES, 87.14 Mb and 273.99 Mb, respectively) and BAC sequences used in this study (2.20 Mb and 1.69 Mb, respectively) were searched against the TIGR Solanum Repeat Database v3.3 using RepeatMasker with a cut-off score of 225. Genomic sequences were quantified based RepeatMasker matches to the TIGR Solanum Repeat Database v3.3 sequences and quantitated at the sub-class level .
Bacterial artificial chromosome
BAC end sequence
Fluorescent in situ hybridization
Long Terminal Repeat
This work was supported by a National Science Foundation Plant Genome Research Program grant to C. R. B. (DBI-0604907). Sequences were generated at the J Craig Venter Institute Joint Technology Center and the assistance of the staff is greatly appreciated. The RHPOTKEY library was provided by Laboratory of Plant Breeding, Wageningen University (Wageningen), Applied Science Foundation STW (Utrecht) and Keygene N.V. (Wageningen).
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